1932

Abstract

The mountain pine beetle epidemic has highlighted the complex interactions of bark beetles with conifer host defenses. In these interactions, oleoresin terpenoids and volatiles, produced and released by the host tree, can be both harmful and beneficial to the beetle's success in colonizing a tree and completing its life cycle. The insect spends almost its entire life, from egg to adult, within the bark and phloem of a pine host, exposed to large quantities of complex mixtures of oleoresin terpenoids. Conifer oleoresin comprises mostly monoterpenes and diterpene resin acids as well as many different sesquiterpenes. It functions as a major chemical and physical defense system. However, the insect has evolved host colonization behavior and enzymes for terpenoid metabolism and detoxification that allow it to overcome some of the terpenoid defenses and, importantly, to co-opt pine monoterpenes as cues for host search and as a precursor for its own pheromone system. The insect-associated microbiome also plays a role in the metabolism of conifer terpenoids.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-070921-103617
2022-05-20
2024-05-11
Loading full text...

Full text loading...

/deliver/fulltext/arplant/73/1/annurev-arplant-070921-103617.html?itemId=/content/journals/10.1146/annurev-arplant-070921-103617&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adams AS, Boone CK, Bohlmann J, Raffa KF. 2011. Responses of bark beetle-associated bacteria to host monoterpenes and their relationship to insect life histories. J. Chem. Ecol. 37:8808–17
    [Google Scholar]
  2. 2.
    Adams AS, Currie CR, Cardoza Y, Klepzig KD, Raffa KF. 2009. Effects of symbiotic bacteria and tree chemistry on the growth and reproduction of bark beetle fungal symbionts. Can. J. Res. 39:61133–47
    [Google Scholar]
  3. 3.
    Adams AS, Six DL 2007. Temporal variation in mycophagy and prevalence of fungi associated with developmental stages of Dendroctonus ponderosae (Coleoptera: Curculionidae). Environ. Entomol. 36:164–72
    [Google Scholar]
  4. 4.
    Andersson MN, Grosse-Wilde E, Keeling CI, Bengtsson JM, Yuen MMS et al. 2013. Antennal transcriptome analysis of the chemosensory gene families in the tree killing bark beetles, Ips typographus and Dendroctonus ponderosae (Coleoptera: Curculionidae: Scolytinae). BMC Genom 14:198
    [Google Scholar]
  5. 5.
    Aukema BH, Carroll AL, Zhu J, Raffa KF, Sickley TA, Taylor SW. 2006. Landscape level analysis of mountain pine beetle in British Columbia, Canada: spatiotemporal development and spatial synchrony within the present outbreak. Ecography 29:3427–41
    [Google Scholar]
  6. 6.
    Aw T, Schlauch K, Keeling CI, Young S, Bearfield JC et al. 2010. Functional genomics of mountain pine beetle (Dendroctonus ponderosae) midguts and fat bodies. BMC Genom. 11:215
    [Google Scholar]
  7. 7.
    Bentz BJ, Boone C, Raffa KF. 2015. Tree response and mountain pine beetle attack preference, reproduction and emergence timing in mixed whitebark and lodgepole pine stands. Agric. For. Entomol. 17:4421–32
    [Google Scholar]
  8. 8.
    Bentz BJ, Hood SM, Hansen EM, Vandygriff JC, Mock KE. 2017. Defense traits in the long-lived Great Basin bristlecone pine and resistance to the native herbivore mountain pine beetle. New Phytol 213:2611–24
    [Google Scholar]
  9. 9.
    Bentz BJ, Regniere J, Fettig CJ, Hansen EM, Hayes JL et al. 2010. Climate change and bark beetles of the western United States and Canada: direct and indirect effects. Bioscience 23:74602–13
    [Google Scholar]
  10. 10.
    Bentz BJ, Six DL. 2006. Ergosterol content of fungi associated with Dendroctonus ponderosae and Dendroctonus rufipennis (Coleoptera : Curculionidae, Scolytinae). Ann. Entomol. Soc. Am. 99:2189–94
    [Google Scholar]
  11. 11.
    Bleiker KP, Potter SE, Lauzon CR, Six DL. 2009. Transport of fungal symbionts by mountain pine beetles. Can. Entomol. 141:5503–14
    [Google Scholar]
  12. 12.
    Bleiker KP, Six DL. 2007. Dietary benefits of fungal associates to an eruptive herbivore: potential implications of multiple associates on host population dynamics. Environ. Entomol. 36:61384–96
    [Google Scholar]
  13. 13.
    Bleiker KP, Van Hezewijk BH. 2016. Flight period of mountain pine beetle (Coleoptera: Curculionidae) in its recently expanded range. Environ. Entomol. 45:61561–67
    [Google Scholar]
  14. 14.
    Bohlmann J. 2012. Pine terpenoid defences in the mountain pine beetle epidemic and in other conifer pest interactions: Specialized enemies are eating holes into a diverse, dynamic and durable defence system. Tree Physiol 32:8943–45
    [Google Scholar]
  15. 15.
    Bonnett TR, Robert JA, Pitt C, Fraser JD, Keeling CI et al. 2012. Global and comparative proteomic profiling of overwintering and developing mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae), larvae. Insect Biochem. Mol. Biol. 42:12890–901
    [Google Scholar]
  16. 16.
    Boone CK, Aukema BH, Bohlmann J, Carroll AL, Raffa KF 2011. Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species. Can. J. Res. 41:61174–88
    [Google Scholar]
  17. 17.
    Boone CK, Keefover-Ring K, Mapes AC, Adams AS, Bohlmann J, Raffa KF. 2013. Bacteria associated with a tree-killing insect reduce concentrations of plant defense compounds. J. Chem. Ecol. 39:71003–6
    [Google Scholar]
  18. 18.
    Borden JH, Pureswaran DS, Lafontaine JP. 2008. Synergistic blends of monoterpenes for aggregation pheromones of the mountain pine beetle (Coleoptera: Curculionidae). J. Econ. Entomol. 101:41266–75
    [Google Scholar]
  19. 19.
    Borden JH, Ryker LC, Chong LJ, Pierce HD Jr., Johnston BD, Oehlschlager AC. 1986. Response of the mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae), to five semiochemicals in British Columbia lodgepole pine forests. Can. J. Res. 17:118–28
    [Google Scholar]
  20. 20.
    Bruce TJA, Wadhams LJ, Woodcock CM. 2005. Insect host location: a volatile situation. Trends Plant Sci 10:6269–74
    [Google Scholar]
  21. 21.
    Burke JL, Bohlmann J, Carroll AL. 2017. Consequences of distributional asymmetry in a warming environment: invasion of novel forests by the mountain pine beetle. Ecosphere 8:4e01778
    [Google Scholar]
  22. 22.
    Byers JA, Wood DL, Craig J, Hendry LB 1984. Attractive and inhibitory pheromone produced in the bark beetle, Dendroctonus brevicomis, during host colonization: regulation of inter- and intraspecific competition. J. Chem. Ecol. 10:6861–77
    [Google Scholar]
  23. 23.
    Byers JA, Zhang Q 2012. Chemical ecology of bark beetles in regard to search and selection of host trees. Recent Advances in Entomological Research T Liu, L Kang 150–90 Berlin: Springer
    [Google Scholar]
  24. 24.
    Cale JA, Ding R, Wang F, Rajabzadeh R, Erbilgin N 2019. Ophiostomatoid fungi can emit the bark beetle pheromone verbenone and other semiochemicals in media amended with various pine chemicals and beetle-released compounds. Fungal Ecol 39:285–95
    [Google Scholar]
  25. 25.
    Campbell SA, Borden JH. 2006. Close-range, in-flight integration of olfactory and visual information by a host-seeking bark beetle. Entomol. Exp. Appl. 120:291–98
    [Google Scholar]
  26. 26.
    Campbell SA, Borden JH. 2006. Integration of visual and olfactory cues of hosts and non-hosts by three bark beetles (Coleoptera: Scolytidae). Ecol. Entomol. 31:5437–49
    [Google Scholar]
  27. 27.
    Cano-Ramírez C, López MF, Cesar-Ayala AK, Pineda-Martínez V, Sullivan BT, Zúñiga G 2013. Isolation and expression of cytochrome P450 genes in the antennae and gut of pine beetle Dendroctonus rhizophagus (Curculionidae: Scolytinae) following exposure to host monoterpenes. Gene 520:147–63
    [Google Scholar]
  28. 28.
    Chen F, Tholl D, Bohlmann J, Pichersky E. 2011. The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66:1212–29
    [Google Scholar]
  29. 29.
    Chiu CC, Keeling CI, Bohlmann J. 2017. Toxicity of pine monoterpenes to mountain pine beetle. Sci. Rep. 7:18858
    [Google Scholar]
  30. 30.
    Chiu CC, Keeling CI, Bohlmann J. 2018. Monoterpenyl esters in juvenile mountain pine beetle and sex-specific release of the aggregation pheromone trans-verbenol. PNAS 115:143652–57Describes a biochemical adaptation of beetles to overcome host defenses and co-opt them for pheromone release.
    [Google Scholar]
  31. 31.
    Chiu CC, Keeling CI, Bohlmann J. 2019. Cytochromes P450 preferentially expressed in the antennae of the mountain pine beetle. J. Chem. Ecol. 45:178–86
    [Google Scholar]
  32. 32.
    Chiu CC, Keeling CI, Bohlmann J. 2019. The cytochrome P450 CYP6DE1 catalyzes the conversion of α-pinene into the mountain pine beetle aggregation pheromone trans-verbenol. Sci. Rep. 9:11477
    [Google Scholar]
  33. 33.
    Chiu CC, Keeling CI, Henderson HM, Bohlmann J 2019. Functions of mountain pine beetle cytochromes P450 CYP6DJ1, CYP6BW1 and CYP6BW3 in the oxidation of pine monoterpenes and diterpene resin acids. PLOS ONE 14:e0216753
    [Google Scholar]
  34. 34.
    Clark EL, Carroll AL, Huber DPW 2010. Differences in the constitutive terpene profile of lodgepole pine across a geographical range in British Columbia, and correlation with historical attack by mountain pine beetle. Can. Entomol. 142:06557–73
    [Google Scholar]
  35. 35.
    Clark EL, Huber DPW, Carroll AL. 2012. The legacy of attack: implications of high phloem resin monoterpene levels in lodgepole pines following mass attack by mountain pine beetle, Dendroctonus ponderosae Hopkins. Environ. Entomol. 41:2392–98
    [Google Scholar]
  36. 36.
    Clark EL, Pitt C, Carroll AL, Lindgren BS, Huber DPW. 2014. Comparison of lodgepole and jack pine resin chemistry: implications for range expansion by the mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae). PeerJ 2:e240
    [Google Scholar]
  37. 37.
    Conn JE, Borden JH, Hunt DWA, Holman J, Whitney HS et al. 1984. Pheromone production by axenically reared Dendroctonus ponderosae and Ips paraconfusus (Coleoptera: Scolytidae). J. Chem. Ecol. 10:2281–90
    [Google Scholar]
  38. 38.
    Cooke BJ, Carroll AL. 2017. Predicting the risk of mountain pine beetle spread to eastern pine forests: considering uncertainty in uncertain times. For. Ecol. Manag. 396:11–25
    [Google Scholar]
  39. 39.
    Cullingham CI, Cooke JE, Dang S, Davis CS, Cooke BJ, Coltman DW. 2011. Mountain pine beetle host-range expansion threatens the boreal forest. Mol. Ecol. 20:2157–71
    [Google Scholar]
  40. 40.
    Dickens JC, Payne TL. 1977. Bark beetle olfaction: Pheromone receptor system in Dendroctonus frontalis. J. Insect Physiol. 23:4481–89
    [Google Scholar]
  41. 41.
    Erbilgin N, Cale JA, Hussain A, Ishangulyyeva G, Klutsch JG et al. 2017. Weathering the storm: how lodgepole pine trees survive mountain pine beetle outbreaks. Oecologia 184:469–78
    [Google Scholar]
  42. 42.
    Erbilgin N, Ma C, Whitehouse C, Shan B, Najar A, Evenden M 2014. Chemical similarity between historical and novel host plants promotes range and host expansion of the mountain pine beetle in a naïve host ecosystem. New Phytol 201:3940–50
    [Google Scholar]
  43. 43.
    Ferrenberg S, Kane JM, Mitton JB 2014. Resin duct characteristics associated with tree resistance to bark beetles across lodgepole and limber pines. Oecologia 174:41283–92
    [Google Scholar]
  44. 44.
    Feyereisen R. 2006. Evolution of insect P450. Biochem. Soc. Trans. 34:1252–55
    [Google Scholar]
  45. 45.
    Feyereisen R 2012. Insect CYP genes and P450 enzymes. Insect Molecular Biology and Biochemistry LI Gilbert 236–316 Cambridge, MA: Academic Press
    [Google Scholar]
  46. 46.
    Franceschi VR, Krokene P, Christiansen E, Krekling T 2005. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol 167:2353–76
    [Google Scholar]
  47. 47.
    Geisler K, Jensen NB, Yuen MMS, Madilao L, Bohlmann J 2016. Modularity of conifer diterpene resin acid biosynthesis: P450 enzymes of different CYP720B clades use alternative substrates and converge on the same products. Plant Physiol 171:1152–64
    [Google Scholar]
  48. 48.
    Gilg AB, Tittiger C, Blomquist GJ. 2009. Unique animal prenyltransferase with monoterpene synthase activity. Naturwissenschaften 96:6731–35
    [Google Scholar]
  49. 49.
    Goodsman DW, Erbilgin N, Lieffers VJ. 2012. The impact of phloem nutrients on overwintering mountain pine beetles and their fungal symbionts. Environ. Entomol. 41:3478–86
    [Google Scholar]
  50. 50.
    Hall DE, Yuen MMS, Jancsik S, Quesada AL, Dullat HK et al. 2013. Transcriptome resources and functional characterization of monoterpene synthases for two host species of the mountain pine beetle, lodgepole pine (Pinus contorta) and jack pine (Pinus banksiana). BMC Plant Biol 13:80A comprehensive characterization of monoterpene synthases of two host species of the mountain pine beetle.
    [Google Scholar]
  51. 51.
    Hall DE, Zerbe P, Jancsik S, Quesada AL, Dullat H et al. 2013. Evolution of conifer diterpene synthases: diterpene resin acid biosynthesis in lodgepole pine and jack pine involves monofunctional and bifunctional diterpene synthases. Plant Physiol 161:2600–16The authors characterize diterpene synthases of two host species of the mountain pine beetle.
    [Google Scholar]
  52. 52.
    Hamberger B, Ohnishi T, Hamberger B, Seguin A, Bohlmann J. 2011. Evolution of diterpene metabolism: Sitka spruce CYP720B4 catalyzes multiple oxidations in resin acid biosynthesis of conifer defense against insects. Plant Physiol 157:41677–95
    [Google Scholar]
  53. 53.
    Hartmann T. 1999. Chemical ecology of pyrrolizidine alkaloids. Planta 207:4483–95
    [Google Scholar]
  54. 54.
    Heckel DG. 2014. Insect detoxification and sequestration strategies. Annual Plant Reviews77–114 Chichester, UK: Wiley & Sons
    [Google Scholar]
  55. 55.
    Huber DPW, Gries R, Borden JH, Pierce HD Jr. 2000. A survey of antennal responses by five species of coniferophagous bark beetles (Coleoptera: Scolytidae) to bark volatiles of six species of angiosperm trees. Chemoecology 10:3103–13
    [Google Scholar]
  56. 56.
    Hughes PR. 1973. Effect of alpha-pinene exposure on trans-verbenol synthesis in Dendroctonus ponderosae Hopkins. Naturwissenschaften 60:5261–62
    [Google Scholar]
  57. 57.
    Hughes PR. 1975. Pheromones of Dendroctonus: origin of alpha-pinene oxidation products present in emergent adults. J. Insect Physiol. 21:3687–91
    [Google Scholar]
  58. 58.
    Hunt DWA, Borden JH. 1989. Terpene alcohol pheromone production by Dendroctonus ponderosae and Ips paraconfusus (Coleoptera: Scolytidae) in the absence of readily culturable microorganisms. J. Chem. Ecol. 15:51433–63
    [Google Scholar]
  59. 59.
    Hunt DWA, Borden JH. 1990. Conversion of verbenols to verbenone by yeasts isolated from Dendroctonus ponderosae. J. Chem. Ecol. 16:41385–97
    [Google Scholar]
  60. 60.
    Hunt DWA, Smirle MJ. 1988. Partial inhibition of pheromone production in Dendroctonus ponderosae (Coleoptera: Scolytidae) by polysubstrate monooxygenase inhibitors. J. Chem. Ecol. 14:2529–35
    [Google Scholar]
  61. 61.
    Keeling CI. 2016. Bark beetle research in the postgenomic era. Adv. Insect Phys. 50:265–95
    [Google Scholar]
  62. 62.
    Keeling CI, Bohlmann J. 2006. Diterpene resin acids in conifers. Phytochemistry 67:222415–23
    [Google Scholar]
  63. 63.
    Keeling CI, Bohlmann J. 2006. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:4657–75
    [Google Scholar]
  64. 64.
    Keeling CI, Henderson H, Li M, Dullat HK, Ohnishi T, Bohlmann J 2013. CYP345E2, an antenna-specific cytochrome P450 from the mountain pine beetle, Dendroctonus ponderosae Hopkins, catalyses the oxidation of pine host monoterpene volatiles. Insect Biochem. Mol. Biol. 43:121142–51
    [Google Scholar]
  65. 65.
    Keeling CI, Henderson H, Li M, Yuen M, Clark EL et al. 2012. Transcriptome and full-length cDNA resources for the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major insect pest of pine forests. Insect Biochem. Mol. Biol. 42:8525–36
    [Google Scholar]
  66. 66.
    Keeling CI, Li M, Sandhu HK, Henderson H, Yuen MM, Bohlmann J. 2016. Quantitative metabolome, proteome and transcriptome analysis of midgut and fat body tissues in the mountain pine beetle, Dendroctonus ponderosae Hopkins, and insights into pheromone biosynthesis. Insect Biochem. Mol. Biol. 70:170–83
    [Google Scholar]
  67. 67.
    Keeling CI, Weisshaar S, Ralph SG, Jancsik S, Hamberger B et al. 2011. Transcriptome mining, functional characterization, and phylogeny of a large terpene synthase gene family in spruce (Picea spp.). BMC Plant Biol 11:43
    [Google Scholar]
  68. 68.
    Keeling CI, Yuen MMS, Liao NY, Docking TR, Chan SK et al. 2013. Draft genome of the mountain pine beetle, Dendroctonus ponderosae Hopkins, a major forest pest. Genome Biol. 14:3R27A genomic resource for the mountain pine beetle and other bark beetle species.
    [Google Scholar]
  69. 69.
    Khadempour L, LeMay V, Jack D, Bohlmann J, Breuil C. 2012. The relative abundance of mountain pine beetle fungal associates through the beetle life cycle in pine trees. Microb. Ecol. 64:4909–17
    [Google Scholar]
  70. 70.
    Krokene P 2015. Conifer defense and resistance to bark beetles. Bark Beetles FE Vega, RW Hofstetter 177–207 Cambridge, MA: Academic Press
    [Google Scholar]
  71. 71.
    Leal WS. 2013. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu. Rev. Entomol. 58:373–91
    [Google Scholar]
  72. 72.
    Li XC, Schuler MA, Berenbaum MR. 2007. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu. Rev. Entomol. 52:231–53
    [Google Scholar]
  73. 73.
    Libbey LM, Ryker LC, Yandell KL. 1985. Laboratory and field studies of volatiles released by Dendroctonus ponderosae Hopkins (Coleoptera, Scolytidae). Zeitschrift Angew. Entomol. 100:381–92
    [Google Scholar]
  74. 74.
    López MF, Cano-Ramírez C, Cesar-Ayala AK, Ruiz EA, Zúñiga G 2013. Diversity and expression of P450 genes from Dendroctonus valens LeConte (Curculionidae: Scolytinae) in response to different kairomones. Insect Biochem. Mol. Biol. 43:5417–32
    [Google Scholar]
  75. 75.
    Lusebrink I, Erbilgin N, Evenden ML. 2013. The lodgepole × jack pine hybrid zone in Alberta, Canada: a stepping stone for the mountain pine beetle on its journey east across the boreal forest?. J. Chem. Ecol. 39:91209–20
    [Google Scholar]
  76. 76.
    Lusebrink I, Evenden ML, Blanchet FG, Cooke JEK, Erbilgin N. 2011. Effect of water stress and fungal inoculation on monoterpene emission from an historical and a new pine host of the mountain pine beetle. J. Chem. Ecol. 37:91013–26
    [Google Scholar]
  77. 77.
    Macfarlane WW, Logan JA, Kern WR. 2017. An innovative aerial assessment of Greater Yellowstone Ecosystem mountain pine beetle-caused whitebark pine mortality. Ecol. Appl. 23:2421–37
    [Google Scholar]
  78. 78.
    MacLean M, Nadeau J, Gurnea T, Tittiger C, Blomquist GJ. 2018. Mountain pine beetle (Dendroctonus ponderosae) CYP4Gs convert long and short chain alcohols and aldehydes to hydrocarbons. Insect Biochem. Mol. Biol. 102:11–20
    [Google Scholar]
  79. 79.
    Martin D, Bohlmann J, Gershenzon J, Francke W, Seybold SJ 2003. A novel sex-specific and inducible monoterpene synthase activity associated with a pine bark beetle, the pine engraver, Ips pini. Naturwissenschaften 90:4173–79
    [Google Scholar]
  80. 80.
    Meddens AJH, Hicke JA, Ferguson CA. 2012. Spatiotemporal patterns of observed bark beetle-caused mortality in British Columbia and the western United States. Ecol. Appl. 22:71876–91
    [Google Scholar]
  81. 81.
    Miller DR, Borden JH. 2000. Dose-dependent and species-specific responses of pine bark beetles (Coleoptera: Scolytidae) to monoterpenes in association with pheromones. Can. Entomol. 132:2183–95
    [Google Scholar]
  82. 82.
    Nadeau JA, Petereit J, Tillett RL, Jung K, Fotoohi M et al. 2017. Comparative transcriptomics of mountain pine beetle pheromone-biosynthetic tissues and functional analysis of CYP6DE3. BMC Genom 18:1311
    [Google Scholar]
  83. 83.
    Nelson D, Werck-Reichhart D. 2011. A P450-centric view of plant evolution. Plant J 66:1194–211
    [Google Scholar]
  84. 84.
    Pierce HD, Conn JE, Oehlschlager AC, Borden JH. 1987. Monoterpene metabolism in female mountain pine beetles, Dendroctonus ponderosae Hopkins, attacking ponderosa pine. J. Chem. Ecol. 13:61455–80
    [Google Scholar]
  85. 85.
    Pitman GB, Vité JP, Kinzer GW, Fentiman AF. 1968. Bark beetle attractants: trans-verbenol isolated from Dendroctonus. Nature 218:5137168–69
    [Google Scholar]
  86. 86.
    Pitt C, Robert JA, Bonnett TR, Keeling CI, Bohlmann J, Huber DPW. 2014. Proteomics indicators of the rapidly shifting physiology from whole mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Curculionidae), adults during early host colonization. PLOS ONE 9:10e110673
    [Google Scholar]
  87. 87.
    Progar RA, Gillette N, Fettig CJ, Hrinkevich K. 2013. Applied chemical ecology of the mountain pine beetle. For. Sci. 60:3414–33
    [Google Scholar]
  88. 88.
    Pureswaran DS, Gries R, Borden JH 2004. Antennal responses of four species of tree-killing bark beetles (Coleoptera: Scolytidae) to volatiles collected from beetles, and their host and nonhost conifers. Chemoecology 14:259–66
    [Google Scholar]
  89. 89.
    Pureswaran DS, Gries R, Borden JH, Pierce HDJr. 2000. Dynamics of pheromone production and communication in the mountain pine beetle, Dendroctonus ponderosae Hopkins, and the pine engraver, Ips pini (Say) (Coleoptera: Scolytidae). Chemoecology 10:153–68
    [Google Scholar]
  90. 90.
    Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA et al. 2008. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. Bioscience 58:6501–17
    [Google Scholar]
  91. 91.
    Raffa KF, Berryman AA. 1982. Physiological differences between lodgepole pines resistant and susceptible to the mountain pine beetle and associated microorganisms. Environ. Entomol. 11:2486–92
    [Google Scholar]
  92. 92.
    Raffa KF, Berryman AA. 1983. The role of host plant resistance in the colonization behavior and ecology of bark beetles (Coleoptera: Scolytidae). Ecol. Monogr. 53:127–49
    [Google Scholar]
  93. 93.
    Raffa KF, Mason CJ, Bonello P, Cook S, Erbilgin N et al. 2017. Defence syndromes in lodgepole-whitebark pine ecosystems relate to degree of historical exposure to mountain pine beetles. Plant Cell Environ 40:91791–1806
    [Google Scholar]
  94. 94.
    Rane RV, Walsh TK, Pearce SL, Jermiin LS, Gordon KHJ et al. 2016. Are feeding preferences and insecticide resistance associated with the size of detoxifying enzyme families in insect herbivores?. Curr. Opin. Insect Sci. 13:70–76
    [Google Scholar]
  95. 95.
    Reid ML, Purcell JRC. 2011. Condition-dependent tolerance of monoterpenes in an insect herbivore. Arthropod Plant Interact 5:4331–37
    [Google Scholar]
  96. 96.
    Reid ML, Sekhon JK, LaFramboise LM. 2017. Toxicity of monoterpene structure, diversity and concentration to mountain pine beetles, Dendroctonus ponderosae: Beetle traits matter more. J. Chem. Ecol. 43:4351–61
    [Google Scholar]
  97. 97.
    Ro D-K, Arimura G-I, Lau SYW, Piers E, Bohlmann J 2005. Loblolly pine abietadienol/abietadienal oxidase PtAO (CYP720B1) is a multifunctional, multisubstrate cytochrome P450 monooxygenase. PNAS 102:228060–65
    [Google Scholar]
  98. 98.
    Robert JA, Bonnett T, Pitt C, Spooner LJ, Fraser J et al. 2016. Gene expression analysis of overwintering mountain pine beetle larvae suggests multiple systems involved in overwintering stress, cold hardiness, and preparation for spring development. PeerJ 4:e2109
    [Google Scholar]
  99. 99.
    Robert JA, Pitt C, Bonnett TR, Yuen MMS, Keeling CI et al. 2013. Disentangling detoxification: Gene expression analysis of feeding mountain pine beetle illuminates molecular-level host chemical defense detoxification mechanisms. PLOS ONE 8:11e77777
    [Google Scholar]
  100. 100.
    Rosenberger DW, Venette RC, Maddox MP, Aukema BH. 2017. Colonization behaviors of mountain pine beetle on novel hosts: implications for range expansion into northeastern North America. PLOS ONE 12:5e0176269
    [Google Scholar]
  101. 101.
    Safranyik L, Carroll AL 2006. The biology and epidemiology of the mountain pine beetle in lodgepole pine forests. The Mountain Pine Beetle—A Synthesis of Biology, Management, and Impacts on Lodgepole Pine L Safranyik, WR Wilson 3–66 Victoria, Can: Pac. For. Cent.
    [Google Scholar]
  102. 102.
    Safranyik L, Carroll AL, Régnière J, Langor DW, Riel WG et al. 2010. Potential for range expansion of mountain pine beetle into the boreal forest of North America. Can. Entomol. 142:5415–42
    [Google Scholar]
  103. 103.
    Sharkey TD, Gray DW, Pell HK, Breneman SR, Topper L. 2013. Isoprene synthase genes form a monophyletic clade of acyclic terpene synthases in the TPS-B terpene synthase family. Evolution 67:41026–40
    [Google Scholar]
  104. 104.
    Smith RH. 1961. The fumigant toxicity of three pine resins to Dendroctonus brevicomis and Dendroctonus jeffreyi. J. Econ. Entomol. 54:365–69
    [Google Scholar]
  105. 105.
    Smith RH. 1963. Toxicity of pine resin vapors to three species of Dendroctonus bark beetles. J. Econ. Entomol. 56:6827–31
    [Google Scholar]
  106. 106.
    Song M. 2012. Mountain pine beetle (MPB; Dendroctonus ponderosae) pheromone component biosynthesis, cytochromes P450 and monoterpene metabolism in bark beetles PhD Thesis Univ. Nev. Reno:
    [Google Scholar]
  107. 107.
    Stamopoulos DC, Damos P, Karagianidou G 2007. Bioactivity of five monoterpenoid vapours to Tribolium confusum (du Val) (Coleoptera: Tenebrionidae). J. Stored Prod. Res. 43:4571–77
    [Google Scholar]
  108. 108.
    Sturgen K, Robertson JL. 1985. Microsomal polysubstrate monooxygenase activity in western and mountain pine beetles. Ann. Entomol. Soc. Am. 78:11–4
    [Google Scholar]
  109. 109.
    Sullivan BT. 2016. Semiochemicals in the natural history of southern pine beetle Dendroctonus frontalis Zimmermann and their role in pest management. Adv. Insect Physiol. 50:Suppl. C129–93
    [Google Scholar]
  110. 110.
    Taft S, Najar A, Erbilgin N 2015. Pheromone production by an invasive bark beetle varies with monoterpene composition of its naïve host. J. Chem. Ecol. 41:540–49
    [Google Scholar]
  111. 111.
    Taft S, Najar A, Godbout J, Bousquet J, Erbilgin N. 2015. Variations in foliar monoterpenes across the range of jack pine reveal three widespread chemotypes: implications to host expansion of invasive mountain pine beetle. Front. Plant Sci. 6:342
    [Google Scholar]
  112. 112.
    Tak J-H, Jovel E, Isman MB 2016. Contact, fumigant, and cytotoxic activities of thyme and lemongrass essential oils against larvae and an ovarian cell line of the cabbage looper, Trichoplusia ni. J. Pest Sci. 89:1183–93
    [Google Scholar]
  113. 113.
    Tholl D. 2015. Biosynthesis and biological functions of terpenoids in plants. Biotechnology of Isoprenoids. Advances in Biochemical Engineering/BiotechnologyVol. 148ed. J Schrader, J Bohlmann Springer, Cham. https://doi.org/10.1007/10_2014_295
    [Crossref] [Google Scholar]
  114. 114.
    Tillman JA, Holbrook GL, Dallara PL, Schal C, Wood DL et al. 1998. Endocrine regulation of de novo aggregation pheromone biosynthesis in the pine engraver, Ips pini (Say) (Coleoptera: Scolytidae). Insect Biochem. Mol. Biol. 28:9705–15
    [Google Scholar]
  115. 115.
    Tittiger C, Blomquist GJ. 2017. Pheromone biosynthesis in bark beetles. Curr. Opin. Insect Sci. 24:68–74
    [Google Scholar]
  116. 116.
    Vanderwel D, Oehlschlager AC. 1992. Mechanism of brevicomin biosynthesis from (Z)-6-nonen-2-one in a bark beetle. J. Am. Chem. Soc. 114:135081–86
    [Google Scholar]
  117. 117.
    Vité JP, Pitman GB. 1968. Bark beetle aggregation: effects of feeding on the release of pheromones in Dendroctonus and Ips. Nature 218:5137169–70
    [Google Scholar]
  118. 118.
    Vogt RG. 2005. Molecular basis of pheromone detection in insects. Compr. Insect Physiol. Biochem. Pharmacol. 3:753–804
    [Google Scholar]
  119. 119.
    Wang Y, Lim L, Diguistini S, Robertson G, Bohlmann J, Breuil C. 2013. A specialized ABC efflux transporter GcABC-G1 confers monoterpene resistance to Grosmannia clavigera, a bark beetle-associated fungal pathogen of pine trees. New Phytol 197:3886–98
    [Google Scholar]
  120. 120.
    Wang Y, Lim L, Madilao L, Lah L, Bohlmann J, Breuil C. 2014. Gene discovery for enzymes involved in limonene modification or utilization by the mountain pine beetle-associated pathogen Grosmannia clavigera. Appl. Environ. Microbiol. 80:154566–76
    [Google Scholar]
  121. 121.
    Warren RL, Keeling CI, Yuen MMS, Raymond A, Taylor GA et al. 2015. Improved white spruce (Picea glauca) genome assemblies and annotation of large gene families of conifer terpenoid and phenolic defense metabolism. Plant J 83:2189–212
    [Google Scholar]
  122. 122.
    Werck-Reichhart D, Feyereisen R. 2000. Cytochromes P450: a success story. Genome Biol 1:6reviews3003.1
    [Google Scholar]
  123. 123.
    White RA, Agosin M, Franklin RT, Webb JW 1980. Bark beetle pheromones: evidence for physiological synthesis mechanisms and their ecological implications. Zeitschrift Angew. Entomol. 90:255–74
    [Google Scholar]
  124. 124.
    Whitehead AT. 1981. Ultrastructure of sensilla of the female mountain pine beetle, Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae). Int. J. Insect Morphol. Embryol. 10:119–28
    [Google Scholar]
  125. 125.
    Whitehill JGA, Bohlmann J. 2019. A molecular and genomic reference system for conifer defense against insects. Plant Cell Environ. 42:2844–59
    [Google Scholar]
  126. 126.
    Zhao S, Klutsch JG, Cale JA, Erbilgin N. 2019. Mountain pine beetle outbreak enhanced resin duct-defenses of lodgepole pine trees. For. Ecol. Manag. 441:271–79
    [Google Scholar]
  127. 127.
    Zulak KG, Bohlmann J. 2010. Terpenoid biosynthesis and specialized vascular cells of conifer defense. J. Integr. Plant Biol. 52:186–97
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-070921-103617
Loading
/content/journals/10.1146/annurev-arplant-070921-103617
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error